Distinct fine‐scale fMRI activation patterns of contra‐ and ipsilateral somatosensory areas 3b and 1 in humans

Stringer, Elizabeth; Qiao, Peng Gang; Friedman, Robert M.; Holroyd, Lauren; Newton, Allen T.; Gore, John C.; Chen, Li Min

doi:10.1002/hbm.22517

Cited by 41 publications

(36 citation statements)

References 81 publications

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“…Figure 3a shows the averaged (n = 20) activation maps for the index (red) and middle (water blue) fingers. In consistent with the previous studies (Ann Stringer et al, 2014;Martuzzi et al, 2014), we found that the middle finger was localized to a more superior position than index finger.…”

Section: Somatotopic Mapping For Right Index and Middle Fingerssupporting

confidence: 93%

Different activation signatures in the primary sensorimotor and higher-level regions for haptic three-dimensional curved surface exploration

Yang

Molfese

et al. 2020

Preprint

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Haptic object perception begins with continuous exploratory contacts, and the human brain needs to accumulate sensory information continuously over time. However, it is still unclear how the primary sensorimotor cortex (PSC) interacts with these higher-level regions during haptic exploration across time. This functional magnetic resonance imaging (fMRI) study investigates time-dependent haptic object processing by examining brain activity during haptic 3D curve and roughness estimation. For this experiment, we designed sixteen haptic stimuli (4 kinds of curve × 4 kinds of roughness) for the haptic curve and roughness estimation tasks. Twenty participants were asked to move their right index and middle fingers along with the surface twice and to estimate one of the two features--roughness or curvature--dependent on the task instruction. We found that the brain activity in several higher-level regions (e.g., bilateral posterior parietal cortex) linearly increased with curvature through the haptic exploration phase. Surprisingly, we found that the contralateral PSC was parametrically modulated by the number of curves only during the late exploration phase, but not during the early exploration phase. In contrast, we found no similar parametric modulation activity patterns for haptic roughness estimation in either the contralateral PSC or in the higher-level regions. Together, our findings suggest that haptic 3D object perception is processed across the cortical hierarchy, while the contralateral PSC interacts with other higher-level regions across time in a manner that is dependent upon object features.HighlightsWe observed the brain activity of haptic object perception using parametric stimuli.Haptic curve estimation showed parametric modulation across the cortical hierarchy.Curve parametric modulation in the sensorimotor cortex showed time dependency.Roughness parametric modulation showed very little dependency in any regions of the brain.These findings reflect the nature of time-dependent haptic object processing in the brain.

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Section: Somatotopic Mapping For Right Index and Middle Fingerssupporting

confidence: 93%

Different activation signatures in the primary sensorimotor and higher-level regions for haptic three-dimensional curved surface exploration

Yang

Molfese

et al. 2020

Preprint

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“…Peripheral nerve injury can enhance activity in ipsilateral S1 (Fornander et al, 2016), especially at the level of interneurons in laminae V and VI (Pelled et al, 2009). Crucially, ipsilateral activations and deactivations in S1 are diffused and not somatotopically specific (Helmich et al, 2005; Reed et al, 2011; Ann Stringer et al, 2014; Geva et al, 2017). They can modulate the amplitude of the S1 response (which is not of interest here), but there is no evidence that they affect the spatial (somatotopic) organisation of the contralateral responses (Reed et al, 2011; Ann Stringer et al, 2014; Geva et al, 2017).…”

Section: Methodsmentioning

confidence: 99%

“…Crucially, ipsilateral activations and deactivations in S1 are diffused and not somatotopically specific (Helmich et al, 2005; Reed et al, 2011; Ann Stringer et al, 2014; Geva et al, 2017). They can modulate the amplitude of the S1 response (which is not of interest here), but there is no evidence that they affect the spatial (somatotopic) organisation of the contralateral responses (Reed et al, 2011; Ann Stringer et al, 2014; Geva et al, 2017). This is further confirmed by our preliminary imaging data, in which we found that unilateral vs. bilateral fingertip mapping yielded both greatly similar and highly reproducible fingertip maps in S1 (Figure 1).…”

Section: Methodsmentioning

confidence: 99%

Fine-grained mapping of cortical somatotopies in chronic Complex Regional Pain Syndrome

Mancini

Wang

Schira

et al. 2018

Preprint

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32It has long been thought that severe chronic pain conditions, such as Complex Regional 33 Pain Syndrome (CRPS), are not only associated with, but even maintained by a 34 reorganisation of the somatotopic representation of the affected limb in primary 35 somatosensory cortex (S1). This notion has driven treatments that aim to restore S1 36 representations, such as sensory discrimination training and mirror therapy. However, 37 this notion is based on both indirect and incomplete evidence obtained with imaging 38 methods with low spatial resolution. Here, we used functional MRI to characterize the S1 39 representation of the affected and unaffected hand in patients with unilateral CRPS. At 40 the group level, the cortical area, location, and geometry of the S1 representation of the 41 CRPS hand were largely comparable to those of the healthy hand and controls. 42However, the area of the map of the affected hand was modulated by disease duration 43 (the smaller the map, the more chronic the CRPS), but not by pain intensity, pain 44 sensitivity and severity of the physical disability. Thus, if any map reorganization occurs, 45it does not appear to be directly related to our pain measures. These findings compel us 46 to reconsider the cortical mechanisms underlying CRPS and the rationale for 47 interventions that aim to "restore" somatotopic representations to treat pain. 49Significance statement 50 51This study shows that the spatial map of the fingers in S1 is largely preserved in chronic 52 CRPS. Shrinkage of the area of the affected hand map can occur in the most chronic 53 stages of disease. Map shrinkage is related to CRPS duration rather than diagnosis, and 54 is unrelated to how much pain patients experience or to the severity of the physical 55 disability. These findings challenge the rationale for using sensory interventions to treat 56 pain by restoring somatotopic representations in CRPS patients. 58 59 Introduction 60Chronic pain is a highly common and debilitating disorder, that can be associated with 61 functional and morphological changes in the brain. For instance, it has long been 62 thought that some severe chronic pain conditions, such as Complex Regional Pain 63 Syndrome (CRPS), are not only associated with, but even maintained by, maladaptive 64 topographic changes in the primary somatosensory cortex (S1) (Maihofner et al., 2003, 93 quantification of the representation of the fingers (i.e. with exclusion of the thumb) in 94 patients with chronic and unilateral CRPS to the upper limb. We tested whether the S1 95 representation of the fingertips of the affected hand was different from that of the healthy 96 hand of CRPS patients and from controls in terms of its spatial extent, location relative to 97 the central sulcus, and geometry (i.e. variability of the map gradients). 98 99 Materials and Methods 100 101 4 Participants. We recruited 20 adults with unilateral CRPS to the upper limb and 20 102 healthy controls (HC) matched for age, gender and handedness. Each participant gave 103 written inf...

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“…Although the role of ipsilateral M1 in motor control is not fully understood, it has been proposed that unilateral movements produce temporary inhibition of ipsilateral M1, which is thought to restrict motor output to the hemisphere contralateral to the intended movement (Beaule et al, 2012;Buetefisch et al, 2014;Chiou et al, 2013;Kobayashi et al, 2003). Unilateral tactile stimulation also produces facilitation and inhibition in contralateral and ipsilateral somatosensory areas (Stringer et al, 2014). Interestingly, a poorer motor performance in healthy adults during unimanual tasks is associated with less suppression of ipsilateral sensorimotor activation (McGregor et al, 2013).…”

Section: Functional Connectivity In Prhdmentioning

confidence: 99%

Functional Connectivity of Primary Motor Cortex Is Dependent on Genetic Burden in Prodromal Huntington Disease

et al. 2014

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Subtle changes in motor function have been observed in individuals with prodromal Huntington disease (prHD), but the underlying neural mechanisms are not well understood nor is the cumulative effect of the disease (disease burden) on functional connectivity. The present study examined the resting-state functional magnetic resonance imaging (rs-fMRI) connectivity of the primary motor cortex (M1) in 16 gene-negative (NEG) controls and 48 gene-positive prHD participants with various levels of disease burden. The results showed that the strength of the left M1 connectivity with the ipsilateral M1 and somatosensory areas decreased as disease burden increased and correlated with motor symptoms. Weakened M1 connectivity within the motor areas was also associated with abnormalities in long-range connections that evolved with disease burden. In this study, M1 connectivity was decreased with visual centers (bilateral cuneus), but increased with a hub of the default mode network (DMN; posterior cingulate cortex). Changes in connectivity measures were associated with worse performance on measures of cognitive-motor functioning. Short- and long-range functional connectivity disturbances were also associated with volume loss in the basal ganglia, suggesting that weakened M1 connectivity is partly a manifestation of striatal atrophy. Altogether, the results indicate that the prodromal phase of HD is associated with abnormal interhemispheric interactions among motor areas and disturbances in the connectivity of M1 with visual centers and the DMN. These changes may, respectively, contribute to increased motor symptoms, visuomotor integration problems, and deficits in the executive control of movement as individuals approach a manifest diagnosis.

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Distinct fine‐scale fMRI activation patterns of contra‐ and ipsilateral somatosensory areas 3b and 1 in humans

Cited by 41 publications

References 81 publications

Different activation signatures in the primary sensorimotor and higher-level regions for haptic three-dimensional curved surface exploration

Different activation signatures in the primary sensorimotor and higher-level regions for haptic three-dimensional curved surface exploration

Fine-grained mapping of cortical somatotopies in chronic Complex Regional Pain Syndrome

Functional Connectivity of Primary Motor Cortex Is Dependent on Genetic Burden in Prodromal Huntington Disease

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